Cells of the sympathoadrenal lineage: Biological properties as donor tissue for cell-replacement therapies for Parkinson's disease

Brain Research Reviews

Volumn 49, Issue 2, 2005, Pages 343-354

  Fernandez Espejo, Emilio ^a   Armengol, Jose A ^b   Flores, Juan A ^a   Galan Rodriguez, Beatriz ^a   Ramiro, Susana ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

Cathecolamine; Chromaffin; Dopamine; Grafting; Neurodegeneration; Neurotrophic; Paraganglia; Parkinson's disease; Sympathoadrenal

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; IMMUNOSUPPRESSIVE AGENT; LEVODOPA; NORADRENALIN; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE IMMUNOTHERAPY; ADRENAL MEDULLA; ADRENERGIC SYSTEM; AUTOGRAFT; AUTOLOGOUS STEM CELL TRANSPLANTATION; BRAIN TRANSPLANTATION; CELL SURVIVAL; CHROMAFFIN CELL; CLINICAL TRIAL; DENERVATION; DYSKINESIA; FLUORESCENCE; GRAFT REJECTION; HUMAN; HYPOXIA; IMMUNOSUPPRESSIVE TREATMENT; NEURAL CREST; NONHUMAN; PARENCHYMA; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SURVIVAL RATE; SYMPATHETIC GANGLION; SYMPATHETIC NERVE CELL;

ADRENAL MEDULLA; ANIMALS; BRAIN TISSUE TRANSPLANTATION; CHROMAFFIN CELLS; GANGLIA, SYMPATHETIC; HUMANS; NEURONS; PARKINSON DISEASE; REPLANTATION; TISSUE THERAPY;

EID: 23844538163     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2005.01.004     Document Type: Review

References (112)

1. M. Ahonen, S. Soinila, and T.H. Joh Pre-and postnatal development of rat retroperitoneal paraganglia J. Auton. Nerv. Syst. 18 1987 11 120
2. D.J. Anderson, and R. Axel Molecular probes for the development and plasticity of neural crest derivatives Cell 42 1985 649 662
3. V. Arjona, A. Minguez-Castellanos, R.J. Montoro, A. Ortega, F. Escamilla, J.J. Toledo-Aral, R. Pardal, S. Mendez-Ferrer, J.M. Martin, M. Perez, M.J. Katati, E. Valencia, T. Garcia, and J. Lopez-Barneo Autotransplantation of human carotid body cell aggregates for treatment of Parkinson's disease Neurosurgery 53 2003 321 328
4. J.A. Armengol Invasive strategies as therapeutic approaches for central nervous system diseases J.M. Delgado-Garcia T. Herdegen Brain damage and repair 2004 Kluwer Academic Press Netherlands 403 421
5. S.M. Baby, A. Roy, A.M. Mokashi, and S. Lahiri Effects of hypoxia and intracellular iron chelation on hypoxia-inducible factor-1alpha and-1beta in the rat carotid body and glomus cells Histochem. Cell Biol. 120 2003 343 352
6. E.O. Backlund, P.O. Granberg, B. Hambeger, E. Knutsson, A. Martensson, G. Sedvall, A. Seiger, and L. Olson Transplantation of adrenal medullary tissue to striatum in parkinsonism J. Neurosurg. 62 1985 169 173
7. K.S. Bankiewicz, M. Palmatie, R.J. Plunkett, A. Cummins, and E.H. Oldfield Reversal of hemiparkinsonian syndrome in nonhuman primates by amnion implantation into caudate nucleus J. Neurosurg. 81 1994 869 876
8. P.E. Batchelor, G.T. Liberatore, J.Y.F. Wong, M.J. Porritt, F. Frerichs, G.A. Donnan, and D.W. Howells Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor J. Neurosci. 19 1999 1708 1716
9. K.D. Beck, J. Valverde, T. Alexi, K. Poulsen, B. Moffat, R.A. Vandlen, A. Rosenthal, and F. Hefti Mesencephalic dopaminergic neurons protected by GDNF from axotomy-induced degeneration in the adult brain Nature 373 1995 339 341
10. A. Björklund, S.B. Dunnett, U. Stenevi, M.E. Lewis, and S.D. Iversen Reinnervation of the denervated striatum by substantia nigra transplants: functional consequences as revealed by pharmacological and sensorimotor testing Brain Res. 199 1980 307 333
11. L.M. Bjorklund, R. Sanchez-Pernaute, S. Chung, T. Andersson, I.Y. Chen, K.S. McNaught, A.L. Brownell, B.G. Jenkins, C. Wahlestedt, K.S. Kim, and O. Isacson Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model Proc. Natl. Acad. Sci. U. S. A. 99 2002 2344 2349
12. E. Blaugrund, T.D. Pham, V.M. Tennyson, L. Lo, L. Sommer, D.J. Anderson, and M.D. Gershon Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal linea markers and Mash-1-dependence Development 122 1996 309 320
13. M.C. Bohn, M. Goldstein, and I.B. Black Expression of phenylethanolamine N-methyltransferase in rat sympathetic ganglia and extra-adrenal chromaffin tissue Dev. Biol. 89 1982 299 308
14. M.C. Bohn, L.C. Cupit, F. Marciano, and D.M. Gash Adrenal medullary grafts enhance recovery of striatal dopaminergic fibers Science 237 1987 913 916
15. C. Brefel-Courbon Parkinson disease and the noradrenaline system Presse Med. 31 2002 1240 1242
16. M. Bresjenac, J. Sagen, G. Seigel, C.L. Paino, J. Kordower, and D.M. Gash Xenogenic adrenal medulla graft rejection rather than survival leads to increased rat striatal tyrosine hydroxylase immunoreactivity J. Neuropathol. Exp. Neurol. 56 1997 490 498
17. M. Bronner-Fraser, and S. Fraser Developmental potential of avian trunk neural crest cells in situ Neuron 3 1989 189 195
18. M. Bronner-Fraser, and S. Fraser Cell lineage analysis of the avian neural crest Development 2 1991 17 22
19. P. Brundin, and A. Björklund Survival of expanded dopaminergic precursors is critical for clinical trials Nat. Neurosci. 1 1998 537
20. P. Brundin, and P. Hagell The neurobiology of cell transplantation in Parkinson's disease Clin. Neurosci. Res. 1 2001 507 520
21. P. Brundin, R.E. Strecker, E. Londos, and A. Björklund Dopamine neurons grafted unilaterally to the nucleus accumbens affect drug-induced circling and locomotion Exp. Brain Res. 69 1987 183 194
22. P. Brundin, J. Karlsson, M. Emgard, G.S. Kaminski Schierle, O. Hansson, A. Petersen, and R.F. Castilho Improving the survival of grafted dopaminergic neurons: a review over current approaches Cell Transplant. 9 2000 179 195
23. M.A. Cenci, I.Q. Whishaw, and T. Schallert Animal models of neurological deficits: how relevant is the rat? Nat. Rev., Neurosci. 3 2002 574 579
24. P. Claude, I.M. Parada, K.A. Gordon, P.A. D'Amore, and J.A. Wagner Acidic fibroblast growth factor stimulates adrenal chromaffin cells to proliferate and to extend neurites, but is not a long-term survival factor Neuron 1 1988 783 790
25. S.V. Conde, T.C. Monteiro, A. Obeso, E.C. Monteiro, R. Rigual, J. Prieto-Lloret, J.A. Ribeiro, and C. Gonzalez Funcion de los quimiorreceptores del cuerpo carotideo en el envejecimiento Rev. Neurol. 37 2003 1131
26. R.E. Coupland The development and fate of catecholamine-secreting endocrine cells H. Parvez S. Parvez Biogenic amines in development 1980 Elsevier Amsterdam 3 28
27. R.E. Coupland The natural history of the chromaffin cell-twenty-five years on the beginning Arch. Histol. Cytol. 52 1989 331 341
28. F. Deimling, S. Finotto, K. Lindner, B. Brühl, J.L. Roig-Lopez, J.E. Garcia-Arraras, C. Goridis, K. Krieglstein, and K. Unsicker Characterization of adrenal chromaffin progenitor cells in mice Adv. Pharmacol. 42 1998 932 935
29. M. Derer, O. Grynszpan-Winograd, and M.M. Portier Immunocytochemical localization of the intermediate filament protein peripherin in adult mouse adrenal chromaffin cells in culture Neuroscience 31 1989 471 477
30. G. Doucet, Y. Murata, P. Brundin, O. Bosler, N. Mons, M. Geffard, C.C. Ouimet, and A. Bjorklund Host afferents into intrastriatal transplants of fetal ventral mesencephalon Exp. Neurol. 106 1989 1 19
31. A.J. Doupe, S.C. Landis, and P.H. Patterson Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors and chromaffin cell plasticity J. Neurosci. 5 1985 2119 2142
32. A.J. Doupe, P.H. Patterson, and S.C. Landis Small intensely fluorescent cells in culture: role of glucocorticoids and growth factors in their development and interconversions with other neural crest derivatives J. Neurosci. 5 1985 2143 2160
33. S. Dunnett, and A. Björklund Prospects for new restorative and neuroprotective treatments in Parkinson's disease Nature 399 1999 A32 A39
34. U. Ernsberger, H. Patzke, J.P. Tissier-Seta, T. Reh, C. Goridis, and H. Rohrer The expression of tyrosine hydroxylase and the transcription factors Phox2 and Cash-1: evidence for distinct inductive steps in the differentiation of chick sympathetic precursor cells Mech. Dev. 52 1995 125 136
35. E. Fernández-Espejo Pathogenesis of Parkinson's disease: prospects of neuroprotective and restorative therapies Mol. Neurobiol. 29 2004 15 30
36. E. Fernández-Espejo, R.J. Montoro, J.A. Armengol, and J. López-Barneo Cellular and functional recovery of parkinsonian rats after intrastriatal transplantation of carotid body cell aggregates Neuron 20 1998 197 206
37. E. Fernández-Espejo, M.C. Gonzalez-Albo, J.P. Moraes, F. El Banoua, J.A. Flores, and I. Caraballo Functional regeneration in a rat Parkinson's model after intrastriatal grafts of GDNF and TGF-β1-expressing extra-adrenal chromaffin cells of the Zuckerkandl's organ J. Neurosci. 21 2001 9888 9895
38. E. Fernández-Espejo, F. El Banoua, B. Galan-Rodriguez, and J.A. Flores Intrastriatal transplantation of extra-adrenal chromaffin cells exerts a trophic restorative functional action in both retrograde and intranigral models of Parkinson's disease in rats Abstract of the meeting on new insights on development neurobiology: a symposium in honor of Rosa-Magda Alvarado-Mallart 2004
39. S. Finotto, K. Krieglstein, A. Schober, F. Deimling, K. Lindner, B. Brühl, K. Beier, J. Metz, J.E. Garcia-Arraras, J.L. Roig-Lopez, P. Monaghan, W. Schmid, T.J. Cole, C. Kellendonk, F. Tronche, G. Schutz, and K. Unsicker Analysis of mice carrying targeted mutations of the glucocorticoid receptor gene argues against an essential role of glucocorticoid signalling for generating adrenal chromaffin cells Development 126 1999 2935 2944
40. M.C. Fishman, W.L. Greene, and D. Platika Oxygen chemoreception by carotid body cells in culture Proc. Natl. Acad. Sci. U. S. A. 82 1985 1448 1450
41. W.J. Freed, H. Cannon-Spoor, and E. Krauthamer Intrastriatal adrenal medulla grafts in rats J. Neurosurg. 65 1986 664 670
42. C.R. Freed, P.R. Greene, R.E. Breeze, W.Y. Tsai, W. DuMouchel, R. Kao, S. Dillon, H. Winfield, S. Culver, J.Q. Trojanowski, D. Eidelberg, and S. Fahn Transplantation of embryonic dopamine neurons for severe Parkinson's disease N. Engl. J. Med. 344 2001 710 719
43. D.M. Gash, Z.M. Zhang, and G. Gerhardt Neuroprotective and neurorestorative properties of GDNF Ann. Neurol. 44 1998 G121 S125
44. C.G. Goetz, G.T. Stebbins, H.L. Klawans, W.C. Holler, R.G. Grossman, R.A. Bakay, and R.D. Penn United Parkinson Foundation neurotransplantation registry on adrenal medullary transplants presurgical, and 1-year and 2-year follow-up Neurology 41 1991 1719 1722
45. Q.A. Hervonen Development of catecholamine-storing cells in human fetal paraganglia and adrenal medulla Acta Physiol. Scand. 368 1971 1 94
46. A. Hervonen, and O. Korkala The effect of hypoxia on the catecholamine content of human fetal abdominal paraganglia and adrenal medulla Acta Obstet. Gynecol. Scand. 51 1972 17 24
47. H. Holgert, A. Dagerlind, and T. Hökfelt Phenotype of intraadrenal ganglion neurons during postnatal development in rat J. Comp. Neurol. 371 1996 603 620
48. M.A. Holzwarth, and M.S. Brownfield Serotonin coexists with epinephrine in rat adrenal medulla cells Neuroendocrinology 41 1985 230 236
49. O. Isacson, L.M. Björklund, and J.M. Schumacher Toward full restoration of synaptic and terminal function of the dopaminergic system in Parkinson's disease by stem cells Ann. Neurol. 53 2003 S135 S148
50. F. Javoy, C. Sotelo, A. Herbet, and Y. Agid Specificity of dopaminergic degeneration induced by intracerebral injection of 6-hydroxydopamine in the nigrostriatal system Brain Res. 102 1976 201 215
51. D. Kirik, C. Rosenblad, A. Björklund, and R.J. Mandel Long-term rAAV-mediated gene transfer of GDNF in the rat Parkinson's model: intrastriatal but not intranigral transduction promotes functional regeneration in the lesioned nigrostriatal system J. Neurosci. 20 2000 4686 4700
52. A. Kohn Die paraganglien Arch. Mikrosk. Anat. 52 1903 262 365
53. J.H. Kordower, J.M. Rosenstein, T.J. Collier, M.A. Burke, E.Y. Chen, J.M. Li, L. Martel, A.E. Levey, E.J. Mufson, T.B. Freeman, and C.W. Olanow Functional fetal nigral grafts in a patient with Parkinson's disease: chemoanatomic, ultrastructural, and metabolic studies J. Comp. Neurol. 370 1996 203 230
54. K. Langley, and N.J. Grant Molecular markers of sympathoadrenal cells Cell Tissue Res. 298 1999 185 206
55. S.H. Lee, N. Lumelsky, L. Studer, J.M. Auerbach, and R.D. McKay Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells Nat. Biotechnol. 18 2000 675 679
56. L.F. Lin, D.H. Doherty, J.D. Lile, S. Bektesh, and F. Collins GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons Science 260 1993 1130 1132
57. O. Lindvall Neural transplantation: a hope for patients with Parkinson's disease? NeuroReport 8 1997 iii x
58. O. Lindvall, E.O. Backlund, L. Farde, G. Sedvall, R. Freeman, B. Hoffer, A. Nobin, A. Seiger, and L. Olson Transplantation in Parkinson's disease: two cases of adrenal medullary grafts to the putamen Ann. Neurol. 22 1987 457 468
59. O. Lindvall, Z. Kokaia, and A. Martinez-Serrano Stem cell therapy for human neurodegenerative disorders-how to make it work Nat. Med. 10 2004 S42 S50 (Suppl.)
60. M.R. Luquin, R.J. Montoro, J. Guillen, L. Saldise, R. Insausti, J. Del Río, and J. Lopez-Barneo Recovery of chronic parkinsonian monkeys by autotransplants of carotid body cell aggregates into putamen Neuron 22 1999 743 750
61. R.A. Lyon, M. Titeler, L. Bigornia, and A.S. Schneider D2 dopamine receptors on bovine chromaffin cell membranes: identification and characterization by [3H]N-methylspiperone binding J. Neurochem. 48 1987 631 635
62. Y. Ma, A. Feigin, V. Dhawan, M. Fukuda, Q. Shi, P. Greene, R. Breeze, S. Fahn, C. Freed, and D. Eidelberg Diskynesia after fetal cell transplantation for parkinsonism: a PET study Ann. Neurol. 52 2002 628 634
63. I. Madrazo, R. Drucker-Colin, V. Diaz, J. Martinez-Mata, C. Torres, and J.J. Becerril Open microsurgical autografts of adrenal medulla to the right caudate nucleus in two patients with intractable Parkinson's disease N. Engl. J. Med. 316 1987 831 834
64. T. Mahalik, T. Finger, I. Stromberg, and L. Olson Substantia nigra transplants into denervated striatum of the rat: ultrastructure of graft and host interconnections J. Comp. Neurol. 240 1985 60 70
65. R.J. Mandel, S.K. Spratt, R.O. Snyder, and S.E. Leff Midbrain injection of recombinant adeno-associated virus encoding rat glial cell line-derived neurotrophic factor protects nigral neurons in a progressive 6-hydroxydopamine-induced degeneration model of Parkinson's disease in rats Proc. Natl. Acad. Sci. U. S. A. 94 1997 14083 14088
66. M.R. Matthews Small, intensely fluorescent cells and the paraneuron concept J. Electron. Microsc. Tech. Aig. 12 1989 408 416
67. C. Missale, L. Castelleti, M. Memo, M.O. Carruba, and P.F. Spano Identification and characterization of postsynaptic D1-and D2-dopamine receptors in the cardiovascular system J. Cardiovasc. Pharmacol. 11 1988 643 650
68. N. Nakao, T. Itakura, Y. Uematsu, and N. Komai Transplantation of cultured sympathetic ganglionic neurons into parkinsonian rat brain: survival and function of graft Acta Neurochir. 133 1995 61 67
69. N. Nakao, K. Kakishita, Y. Uematsu, T. Yoshimasu, T. Bessho, K. Nakai, Y. Naito, and T. Itakura Enhancement of the response to levodopa therapy after intrastriatal transplantation of autologous sympathetic neurons in patients with Parkinson disease J. Neurosurg. 95 2001 275 284
70. N. Nakao, A. Shintani-Mizushima, K. Kakishita, and T. Itakura The ability of grafted human sympathetic neurons to synthesize and store dopamine: a potential mechanism for the clinical effect of sympathetic neuron autografts in patients with Parkinson's disease Exp. Neurol. 188 2004 65 673
71. D.T. O'Connor, R.L. Klein, A.K. Thureson-Klein, and J.A. Barbosa Chromogranin A: localization and stoichiometry in large dense core catecholamine storage vesicles from sympathetic nerve Brain Res. 567 1991 188 196
72. C.W. Olanow, T.B. Freeman, and J.H. Kordower Neural transplantation as a therapy for Parkinson's disease Adv. Neurol. 74 1997 246 269
73. R. Pallini, E. Fernandez, L. Lauretti, E. Dell'Anna, F. La Marca, C. Gangitano, A. Delfa, C. Olivieri-Sangiacomo, A. Sbriccoli, and G.F. Rossi Superior cervical ganglion regenerating axons through peripheral nerve grafts and reversal of behavioral deficits in hemiparkinsonian rats J. Neurosurg. 84 1996 487 493
74. D.I. Peterson, M.L. Price, and C.S. Small Autopsy findings in a patient that had and adrenal-to-brain transplant for Parkinson's disease Neurology 39 1988 144
75. P. Piccini, D.J. Brooks, A. Bjorklund, R.N. Gunn, P.M. Grasby, O. Rimoldi, P. Brundin, P. Hagell, S. Rehncrona, H. Widner, and O. Lindvall Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient Nat. Neurosci. 2 1999 1137 1140
76. C. Pupilli, R. Lanzillotti, G. Fiorelli, C. Selli, R.A. Gomez, R.M. Carey, M. Serio, and M. Mannelli Dopamine D2 receptors gene expression and binding sites in adrenal medulla and pheocromocytoma J. Clin. Endocrinol. Metab. 79 1994 56 61
77. D. Purves, W.D. Snider, and J.T. Voyvodic Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system Nature 336 1988 123 128
78. E. Reissmann, U. Ernsberger, P.H. Francis-West, D. Rueger, P.M. Brickell, and H. Rohrer Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons Development 122 1996 2079 2088
79. F. Santagati, and F.M. Rijli Cranial neural crest and the building of the vertebrate head Nat. Rev., Neurosci. 4 2003 806 818
80. B. Schutz, M.K. Shafer, L.E. Eiden, and E. Wheihe Vesicular amine transporter expression and isoform selection in developing brain, peripheral nervous system and gut Brain Res. Dev. Brain Res. 106 1998 181 204
81. R.K.W. Schwarting, and J.P. Huston The unilateral 6-hydroxydopamine lesion model in behavioural brain research. Analysis of functional deficits, recovery and treatments Prog. Neurobiol. 50 1996 275 331
82. F.J. Seidler, and T.A. Slotkin Adrenomedullary function in the neonatal rat: responses to hypoxia J. Physiol. 358 1985 1 16
83. F.J. Seidler, and T.A. Slotkin Ontogeny of adrenomedullary responses to hypoxia and hypoglycemia: role of splachnic innervation Brain Res. Bull. 16 1986 11 14
84. T. A Slotkin, and F.J. Seidler Adrenomedullary catecholamine release in the fetus and newborn: secretory mechanisms and their role in stress and survival J. Dev. Physiol. 10 1988 1 16
85. W.D. Snider Nerve growth factor enhances dendritic arborization of sympathetic ganglion cells in developing mammals J. Neurosci. 8 1988 2628 2634
86. C. Sotelo, F. Javoy, Y. Agid, and J. Glowinski Injection of 6-hydroxydopamine in the substantia nigra of the rat, I. Morphological study Brain Res. 58 1973 269 290
87. J. Srinivasan, and W.J. Schmidt Behavioral and neurochemical effects of noradrenergic depletions with N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine in 6-hydroxydopamine-induced rat model of Parkinson's disease Behav. Brain Res. 151 2004 191 199
88. U. Stenevi, A. Björklund, and N.A. Svendgaard Transplantation of central and peripheral monoamine neurons to the adult rat brain: techniques and conditions for survival Brain Res. 114 1976 1 20
89. L. Studer, V. Tabar, and R.D. McKay Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats Nat. Neurosci. 1 1998 290 295
90. G. Teitelman, S. Skaper, H. Baker, D.H. Park, T.H. Joh, and R. Adler Expression of phenylethanolamine N-methyltransferase in sympathetic neurons and extraadrenal chromaffin tissue of chick embryos in vivo and in vitro Brain Res. 315 1984 283 291
91. L. Testut, and A. Latarjet Tratado de anatomía humana 1978 Salvat Barcelona
92. H. Tian, A.M. McKnight, and D.W. Russell Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells Genes Dev. 11 1997 72 82
93. H. Tian, R.E. Hammer, A.M. Matsumoto, D.W. Russell, and S.L. McKnight The hypoxia-responsive transcription factor EPAS1 is essential for cathecolamine homeostasis and protection against heart failure during embryonic development Genes Dev. 12 1998 3320 3324
94. A.S. Tischler The adrenal medulla and extra-adrenal paraganglia K. Kovacs S.L. Asa Functional endocrine pathology 1990 Blackwell Cambridge, MA
95. A.S. Tischler Chromaffin cells as models of endocrine cells and neurons Ann. N. Y. Acad. Sci. 971 2002 366 370
96. J.J. Toledo-Aral, S. Mendez-Ferrer, R. Pardal, M. Echevarria, and J. Lopez-Barneo Trophic restoration of the nigrostriatal dopaminergic pathway in long-term carotid body-grafted parkinsonian rats J. Neurosci. 23 2003 141 148
97. A. Tomac, E. Lindqvist, L.F. Lin, S.O. Ogren, D. Young, B.J. Hoffer, and L. Olson Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo Nature 373 1995 335 339
98. J.M. Trifaro Molecular biology of the chromaffin cell Ann. N. Y. Acad. Sci. 971 2002 11 18
99. J.L. Tseng, E.E. Baetge, A.D. Zurn, and P. Aebisher GDNF reduces drug-induced rotational behavior after medial forebrain bundle transection by a mechanisms not involving striatal dopamine J. Neurosci. 17 1997 325 333
100. U. Ungerstedt, and G.W. Arbuthnott Quantitative recording of rotational behavior in rats after 6-hydroxydopamine lesions of the nigrostriatal dopamine system Brain Res. 24 1970 486 493
101. K. Unsicker The chromaffin cell: paradigm in cell, developmental and growth factor biology J. Anat. 183 1993 207 221
102. K. Unsicker The trophic cocktail made by adrenal chromaffin cells Exp. Neurol. 123 1993 167 173
103. K. Unsicker, and K. Krieglstein Growth factors in chromaffin cells Prog. Neurobiol. 48 1996 307 324
104. K. Unsicker, S.D. Skaper, and S. Varon Developmental changes in the responses of rat chromaffin cells to neurotrophic and neurite-promoting factors Dev. Biol. 111 1985 425 433
105. K. Unsicker, B. Krisch, J. Otten, and H. Thoenen Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids Proc. Natl. Acad. Sci. 75 1978 3498 3502
106. K. Unsicker, S. Finotto, and K. Krieglstein Generation of cell diversity in the peripheral autonomic nervous system: the sympathoadrenal cell lineage revisited Ann. Anat. 179 1997 495 500
107. I. Valarche, J.P. Tissier-Seta, M.R. Hirsch, S. Martinez, C. Goridis, and J.F. Brunet The mouse homeodomain protein Phox2 regulates Ncam promoter activity in concert with Cux/CDP and is a putative determinant of neurotransmitter phenotype Development 119 1993 881 896
108. K.S. Vogel, and J.A. Weston The sympathoadrenal lineage in avian embryos. I. Adrenal chromaffin cells loose neuronal traits during embryogenesis Dev. Biol. 139 1990 1 12
109. M.S. Wiesener, H. Turley, W.E. Allen, C. William, K.U. Eckardt, K.L. Talks, S.M. Wood, K.C. Gatter, A.L. Harris, C.W. Pugh, P.J. Ratcliffe, and P.H. Maxwell Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha Blood 92 1998 2260 2268
110. H. Winkler, D.K. Apps, and R. Fischler-Colbrie The molecular function of adrenal chromaffin cell granules: established facts and unresolved topics Neuroscience 18 1986 261 290
111. L.I. Xue-Kun, G.U.O. An-Chen, and Z.U.O. Ping-Ping Survival and differentiation of transplanted neural stem cells in mice brain with MPTP-induced Parkinson disease Acta Pharmacol. Sin. 24 2003 1192 1198
112. E. Zuckerkandl Ueber nebenorgane des sympathicus in Retroperitonealraum des menschen Verh Anat. Ges. 15 1901 85 107